Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC

ABSTRACT Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other ba...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Andrew N. Gray, Josephine M. Henderson-Frost, Dana Boyd, Shirin Shirafi, Hironori Niki, Marcia B. Goldberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/01cb95483d334dd88d90b437c11f0435
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:01cb95483d334dd88d90b437c11f0435
record_format	dspace
spelling	oai:doaj.org-article:01cb95483d334dd88d90b437c11f04352021-11-15T15:38:48ZUnbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC10.1128/mBio.00238-112150-7511https://doaj.org/article/01cb95483d334dd88d90b437c11f04352011-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00238-11https://doaj.org/toc/2150-7511ABSTRACT Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other bacteria, Archaea, mitochondria, and chloroplasts, functions by incompletely understood mechanisms in the insertion and folding of certain membrane proteins. Using a genome-scale approach, we identified 69 E. coli membrane proteins that, in the absence of YidC, exhibited aberrant localization by microscopy. Further examination of a subset revealed biochemical defects in membrane insertion in the absence of YidC, indicating their dependence on YidC for proper membrane insertion or folding. Membrane proteins possessing an unfavorable distribution of positively charged residues were significantly more likely to depend on YidC for membrane insertion. Correcting the charge distribution of a charge-unbalanced YidC-dependent membrane protein abrogated its requirement for YidC, while perturbing the charge distribution of a charge-balanced YidC-independent membrane protein rendered it YidC dependent, demonstrating that charge distribution can be a necessary and sufficient determinant of YidC dependence. These findings provide insights into a mechanism by which YidC promotes proper membrane protein biogenesis and suggest a critical function of YidC in all organisms and organelles that express it. IMPORTANCE Biological membranes are fundamental components of cells, providing barriers that enclose the cell and separate compartments. Proteins inserted into biological membranes serve critical functions in molecular transport, molecular partitioning, and other essential cell processes. The mechanisms involved in the insertion of proteins into membranes, however, are incompletely understood. The YidC protein is critical for the insertion of a subset of proteins into membranes across an evolutionarily wide group of organisms. Here we identify a large group of proteins that depend on YidC for membrane insertion in Escherichia coli, and we identify unfavorable distribution of charge as an important determinant of YidC dependence for proper membrane insertion.Andrew N. GrayJosephine M. Henderson-FrostDana BoydShirin ShirafiHironori NikiMarcia B. GoldbergAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 6 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Andrew N. Gray Josephine M. Henderson-Frost Dana Boyd Shirin Shirafi Hironori Niki Marcia B. Goldberg Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
description	ABSTRACT Membrane proteins are involved in numerous essential cell processes, including transport, gene regulation, motility, and metabolism. To function properly, they must be inserted into the membrane and folded correctly. YidC, an essential protein in Escherichia coli with homologues in other bacteria, Archaea, mitochondria, and chloroplasts, functions by incompletely understood mechanisms in the insertion and folding of certain membrane proteins. Using a genome-scale approach, we identified 69 E. coli membrane proteins that, in the absence of YidC, exhibited aberrant localization by microscopy. Further examination of a subset revealed biochemical defects in membrane insertion in the absence of YidC, indicating their dependence on YidC for proper membrane insertion or folding. Membrane proteins possessing an unfavorable distribution of positively charged residues were significantly more likely to depend on YidC for membrane insertion. Correcting the charge distribution of a charge-unbalanced YidC-dependent membrane protein abrogated its requirement for YidC, while perturbing the charge distribution of a charge-balanced YidC-independent membrane protein rendered it YidC dependent, demonstrating that charge distribution can be a necessary and sufficient determinant of YidC dependence. These findings provide insights into a mechanism by which YidC promotes proper membrane protein biogenesis and suggest a critical function of YidC in all organisms and organelles that express it. IMPORTANCE Biological membranes are fundamental components of cells, providing barriers that enclose the cell and separate compartments. Proteins inserted into biological membranes serve critical functions in molecular transport, molecular partitioning, and other essential cell processes. The mechanisms involved in the insertion of proteins into membranes, however, are incompletely understood. The YidC protein is critical for the insertion of a subset of proteins into membranes across an evolutionarily wide group of organisms. Here we identify a large group of proteins that depend on YidC for membrane insertion in Escherichia coli, and we identify unfavorable distribution of charge as an important determinant of YidC dependence for proper membrane insertion.
format	article
author	Andrew N. Gray Josephine M. Henderson-Frost Dana Boyd Shirin Shirafi Hironori Niki Marcia B. Goldberg
author_facet	Andrew N. Gray Josephine M. Henderson-Frost Dana Boyd Shirin Shirafi Hironori Niki Marcia B. Goldberg
author_sort	Andrew N. Gray
title	Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
title_short	Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
title_full	Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
title_fullStr	Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
title_full_unstemmed	Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC
title_sort	unbalanced charge distribution as a determinant for dependence of a subset of <named-content content-type="genus-species">escherichia coli</named-content> membrane proteins on the membrane insertase yidc
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/01cb95483d334dd88d90b437c11f0435
work_keys_str_mv	AT andrewngray unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc AT josephinemhendersonfrost unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc AT danaboyd unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc AT shirinshirafi unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc AT hironoriniki unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc AT marciabgoldberg unbalancedchargedistributionasadeterminantfordependenceofasubsetofnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentmembraneproteinsonthemembraneinsertaseyidc
_version_	1718427805803347968

Unbalanced Charge Distribution as a Determinant for Dependence of a Subset of <named-content content-type="genus-species">Escherichia coli</named-content> Membrane Proteins on the Membrane Insertase YidC

Ejemplares similares